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Haplogroup C seems to have come into existence shortly after M168 was introduced, probably at least 60,000 years before present. Although Haplogroup C attains its highest frequencies among the indigenous populations of Mongolia, the Russian Far East, Polynesia, Australia, and at moderate frequency in the Korean Peninsula and Manchuria, it displays its highest diversity among modern populations of India, and therefore it is hypothesized that Haplogroup C either originated or underwent its longest period of evolution and diversification within India or the greater South Asian coastal region.

It represents a great coastal migration along Southern Asia, into Southeast Asia and Australia, and up the Asian coast. It is believed to have migrated to the Americas some 6,000-8,000 years before present, and was carried by Na-Dené speaking peoples into the northwest Pacific coast of America. Some have hypothesized that Haplogroups C and D were brought together to East Asia by a single population that became the first successful modern human colonizers of that region, but at present the distributions of Haplogroups C and D are different, with various subtypes of Haplogroup C being found at high frequency among the Australian aborigines, Polynesians, Vietnamese, Kazakhs, Mongolians, Manchurians, Koreans, and indigenous inhabitants of the Russian Far East and at moderate frequencies elsewhere throughout Asia and Oceania, including India and Southeast Asia, whereas Haplogroup D is found at high frequencies only among the Tibetans, Japanese peoples, and Andaman Islanders, and has been found neither in India nor among the aboriginal inhabitants of the Americas or Oceania.

Haplogroup C contains the polymorphism, very common in Central Asia, which is believed to be that of Genghis Khan, spread wide during the Mongol conquest of Asia.

The distribution of Haplogroup C is generally limited to populations of northern Eurasia, eastern Eurasia, Oceania, and the Americas. There is a tendency for Haplogroup C to appear as the minor component of Y-chromosome diversity among a population in which the major component is accounted for by subclades of Haplogroup K (M9). Haplogroup C also rarely co-occurs with Haplogroup D among populations of northern Eurasia.

Due to the tremendous age of this macro-haplogroup, numerous mutations have had time to accumulate on the background of a Haplogroup C-M130 Y-chromosome, and several regionally important subbranches of Haplogroup C have been identified. Haplogroup C3-M217 is probably the most important of these, as the geographic extent of its dispersal is without compare, stretching longitudinally from regional subgroups of the Germans in Central Europe all the way to the Wayuu people in northern Colombia and northwest Venezuela, and latitudinally from the Evens and Koryaks of the Russian Far East and the Athabaskan peoples of Alaska and western Canada all the way to Turkey, Pakistan, Vietnam, and the Malay Archipelago. The highest frequencies of Haplogroup C3 are found among the populations of Mongolia and the Russian Far East, where it is generally the modal haplogroup. Haplogroup C3 is the only variety of Haplogroup C to be found among Native Americans, among whom it reaches its highest frequency in Na-Dené populations.

Other distinctive subbranches of Haplogroup C have been found to be specific to certain populations within restricted geographical territories, and even where these other branches are found, they tend to appear as a very low-frequency, minor component of the palette of Y-chromosome diversity within those territories. Haplogroup C1, a very ancient but at present extremely rare lineage, is specific to the Japanese and Ryukyuan populations of Japan, among whom it occurs at a frequency of about 5.4%. Haplogroup C2 is found among certain local populations within Indonesia, Melanesia, Micronesia, and Polynesia; among the populations of some islands of Polynesia, Haplogroup C2 has become the modal haplogroup, probably due to severe founder effects and genetic drift. The recently identified Haplogroup C4 is the most common haplogroup among indigenous Australians, and it has not been found outside of that continent. Haplogroup C5 occurs at a very low frequency in India, Nepal, and Pakistan.

Patrilines that belong to Haplogroup C but do not belong to any of its identified subgroups are labeled as Haplogroup C*, which are found at low frequencies along the southern coast of Asia from India to Vietnam and into the interior of Yunnan province in China, as well as throughout the Philippines, Indonesia, and Micronesia. Haplogroup C* Y-chromosomes have also been detected, but only at even lower frequencies, among populations of coastal New Guinea and island Melanesia; this suggests that, within Oceania, Haplogroup C* is associated with populations of Austronesian cultural affiliation, despite the fact that the derived haplogroup C4 is predominant among the indigenous inhabitants of Australia. Several examples of Haplogroup C*, which appear to be closely related to a scatter of modern South Asian C* haplotypes, have also been found at vanishingly low frequency among the Turkic peoples of Central Asia. Some researchers have also reported finding a Haplogroup C-RPS4Y Y-chromosome in a Lebanese man with a sample size of only 31 individuals (i.e., 1/31 or approximately 3.2%), but it is not clear whether this was really a C* chromosome, in which case descent from a South Asian immigrant might be indicated, or whether it belonged to an identified subclade of Haplogroup C, such as C3, which would make it more likely that this particular Lebanese man descended from a Turco-Mongol invader.